He was in favour of Brexit during the 2016 EU membership referendum.[3] Following the referendum, which resulted in a narrow majority in favour of Brexit, he was one of several Conservative MPs who signed a letter to Theresa May demanding a "hard Brexit", which would see the UK withdraw from both the European Single Market and the Customs Union.[16]

In April 2011, he called for a public inquiry into phone hacking at the News of the World and to why a series of investigations by Scotland Yard failed to link any News International employees to phone hacking other than the News of the World's former royal editor, Clive Goodman. Whittingdale said: "There are some very big questions; what I find [most] worrying is the apparent unwillingness of the police, who had the evidence and chose to do nothing with it. That's something that needs to be looked into."[19]

With just one out of three of News International's senior executives agreeing to appear before the committee session on 19 July, Whittingdale took the rarely used step of issuing a summons to compel the Murdochs to attend.[20] Whittingdale said Select Committees had taken such steps against individuals in the past and they had complied and continued "I hope very much that the Murdochs will respond similarly."[21] They both did, on 19 July, in what one paper described as the most important Select Committee hearing in parliamentary history.[22]

In 2012, Whittingdale received £8,000 for 32 hours' work as a non-executive director of Audio Network plc, an online music catalogue.[23] He was also reimbursed expenses for official visits to Yalta, Taiwan and Armenia.[23]

In April 2016, Shadow Culture Secretary Maria Eagle called for Whittingdale to recuse himself from decisions regarding the outcome of the Leveson Inquiry into press ethics because the story about Whittingdale's former girlfriend being a sex worker exposed him to pressure from the press.[25] A week later, it emerged that Whittingdale had accepted hospitality from the Lap Dancing Association in about 2008 at which time Whittingdale and two other MPs visited two clubs in one evening, while the industry's licensing was under investigation by the Culture, Media and Sport select committee. The hospitality was not declared in the Register of members' interests, or later when Whittingdale later spoke out in the Commons against new regulations introduced by the Labour government.[26][27]

On 14 July 2016, Whittingdale was removed from his position as Culture Secretary by the new Prime Minister, Theresa May.[3]

In July 2016, shortly after his sacking, The Guardian criticised Whittingdale over his decision to turn down a request from the Daily Mirror for the release of historic documents relating to Mark Thatcher's dealings with the government of Oman in the 1980s. Roy Greenslade wrote that few, "apart from the man himself and his friends", could disagree with the argument that the public had a right to know.[28]

Whittingdale married Ancilla Campbell Murfitt, a nurse and school governor, in 1990; the couple had two (now adult) children before their divorce.[29][30] Whittingdale's half-brother is Charles Napier, former treasurer of the defunct Paedophile Information Exchange, who was most recently convicted of child sexual abuse offences in November 2014.[31]

On 12 April 2016, British media reported Whittingdale had been involved in a relationship with a female sex worker between August 2013 and February 2014. In a statement to the BBC's Newsnight programme, he said he had been unaware of his girlfriend's true occupation after meeting her through Match.com, and that he had ended the relationship after he had discovered it through reports that the story was being offered for publication to tabloids.[25][32] On 13 April, David Cameron's spokesman said, "John Whittingdale’s view was that this was in the past, and had been dealt with."[33]